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Behavioral thermoregulation in a gregarious lemur Eulemur collaris Effects of climatic and dietary-related factors.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 144:355–364 (2011)
Behavioral Thermoregulation in a Gregarious Lemur,
Eulemur collaris: Effects of Climatic and Dietary-Related
Factors
Giuseppe Donati,1,2* Eva Ricci,2 Nicoletta Baldi,2 Valentina Morelli,2 and Silvana M. Borgognini-Tarli2
1
Nocturnal Primate Research Group, Department of Anthropology and Geography, Oxford Brookes University,
Oxford, OX3 0BP, UK
2
Department of Biology, Unit of Anthropology, University of Pisa, Pisa, Italy
KEY WORDS
Madagascar
Eulemur collaris; thermal ecology; nutritional ecology; canonical correlation;
ABSTRACT
Primates deal with fluctuations of the
thermal environment by both physiological and behavioral mechanisms of thermoregulation. In this article we
focus on nonhibernating lemurs, which are hypometabolic and have to cope with a seasonal environment. Behavioral thermoregulation has received little attention
compared with specific physiological adaptations to seasonality, i.e., hibernation and torpor, which characterize
a number of lemurs. We investigated the role of seasonality and dietary-related factors in determining frequencies of resting, social and postural thermoregulation, and
microhabitat selection in collared lemurs, Eulemur collaris. We observed two groups of collared lemurs over a
14-month period in the littoral forest of Sainte Luce,
Southern Madagascar. Frequencies of total resting and
time spent in huddling, prone, and curled postures were
collected via 5-min instantaneous sampling. Microhabi-
Endothermal animals use a series of behavioral strategies
to supplement autonomic physiological mechanisms of thermoregulation, including activity and postural adjustments,
social thermoregulation, and microhabitat selection (Refinetti, 1998; Seebacher and Franklin, 2005). The first two
strategies include saving energy by reducing activity and
controlling heat-radiation by modifying the body surface/volume ratio, while the latter consists of the active search for a
microhabitat whose thermal conditions approach the thermoneutral zone (Stevenson, 1985), i.e., the range of environmental temperatures over which the heat produced by an
endotherm remains fairly constant. In addition to chemical
thermogenesis and the control of peripheral circulation, behavioral thermoregulation represents an important system
to reduce energy expenditure for thermoregulation, and, in
many species, to minimize body temperature variations in
case of small thermal fluctuations. In mammals supplementary physiological mechanisms (e.g., shiver or perspiration)
are activated when behavioral adaptations are insufficient
or inadequate (Satinoff, 1978).
Among mammals, both nonplacental semi-poikilotherms (McNab, 1978; Rübsamen et al., 1983; Körtner
and Geiser, 2000; McCarron et al., 2001; Brice et al.,
2002; Grigg et al., 2003; Bethge et al., 2004) and placental endotherms (Bradley and Hudson, 1974; Hasler and
Sorenson, 1974) use the full set of behavioral thermoregulatory strategies, although in different combinations
and in different proportions. Primates have been shown
to resort to microhabitat selection, adjustments in posC 2010
V
WILEY-LISS, INC.
tat selection was evaluated as the proportion of time
spent in the upper canopy as compared with other
layers. Climatic variables were recorded by automatic
data loggers, while dietary variables were derived from
phenological data and nutritional analyses of the
ingested food items. We weighted the combined effects of
climatic and dietary variables on the different types of
behavioral thermoregulation by means of canonical correlation analysis. The model with the strongest canonical
correlation included a first root representing mainly
feeding time, day length, and ambient temperature and
a second root representing diet quality and height of
feeding trees. The output indicated that collared lemurs
adapt to thermal and dietary-related metabolic stress by
adjusting resting time, social, and postural thermoregulation. Am J Phys Anthropol 144:355–364, 2011. V 2010
C
Wiley-Liss, Inc.
ture and activity, and huddling as responses to environmental temperature (Microcebus murinus, Aujard et al.,
1998; Varecia variegata, Morland, 1993; Leontopithecus
rosalia, Thompson et al., 1994; Alouatta caraya, BiccaMarquez and Calegaro-Marquez, 1998; Colobus polykomos, Dasilva, 1993; Papio cynocephalus, Stelzner and
Hausfater, 1986; Pochron, 2000; Hill and Dunbar, 2002;
Hill et al., 2004; Hill, 2006; Macaca fuscata, Schino and
Troisi, 1990; Hanya et al., 2007; Cebus capucinus, Campos and Fedigan, 2009; Pan troglodytes, Takemoto, 2004;
Kosheleff and Anderson, 2009).
These studies demonstrate that behavioral thermoregulation represents an important dimension in primate
Grant sponsors: Department of Biology, University of Pisa;
Department of Anthropology and Geography, Oxford Brookes University; Department of Animal Ecology and Conservation, University of Hamburg.
*Correspondence to: Giuseppe Donati, Nocturnal Primate
Research Group, Department of Anthropology and Geography,
Oxford Brookes University, Oxford, OX3 0BP, United Kingdom.
E-mail: gdonati@brookes.ac.uk
Received 1 December 2009; accepted 27 August 2010
DOI 10.1002/ajpa.21415
Published online 26 October 2010 in Wiley Online Library
(wileyonlinelibrary.com).
356
G. DONATI ET AL.
time-budgets. Although relevant literature is available
on social thermoregulation in small mammals (Kauffman
et al., 2003; Kotze et al., 2008), we do not know much
about the relative importance of different forms of behavioral thermoregulation as a reaction to the thermal
environment in primates. A further problem is to identify the role of climatic factors affecting the perception of
external temperature, among them relative humidity,
wind velocity, and solar radiation (Hill et al., 2004). A
high relative humidity, for instance, increases perceived
temperature, because of a decrease in evaporation rate,
while perceived temperature decreases in the presence of
wind because of the higher efficiency of heat loss by convection (Mount, 1979). Also, behavioral thermoregulation
of wild mammals has been mainly analyzed in relation
to climatic variables, while other ecological aspects, such
as dietary-related factors, rarely have been considered.
In fact, nonclimatic variables, such as food availability
and quality, as well as social factors, may have thermoregulatory implications (Dhal and Smith, 1985; Schino
and Troisi, 1990; Dasilva, 1993).
Malagasy lemurs show an extensive set of behavioral,
postural, and social activities which seem to function as
thermoregulatory mechanisms (Richard and Dewar, 1991;
Morland, 1993; Ostner, 2002). This has been interpreted
as a response to the pronounced seasonality and climatic
unpredictability that characterize the Malagasy island
environment (Jolly, 1984; Wright, 1999; Dewar and Richard, 2007). The lemurs studied so far appear to be hypometabolic (Genoud, 2002; Simmen et al., 2010) with limited sweating mechanisms (Aujard et al., 1998), and it has
been suggested that they should often resort to behavioral
thermoregulation (Morland, 1993). In particular, E. fulvus, a sister species of E. collaris, object of this research,
has been shown to have a basal metabolic rate which is
among the lowest in prosimians, ranging from 28 to 56%
of the expected value of the Kleiber equation, coupled
with a relatively constant body temperature (Daniels,
1984; van Schaik and Kappeler, 1996). Therefore, it is reasonable to hypothesize that Eulemur spp. will have a wide
range of mechanisms to ensure temperature homeostasis,
including behavioral strategies.
The aim of this research was to investigate the role of
climatic and dietary-related factors on year-round behavioral thermoregulation in two groups of collared lemurs
living in a littoral forest fragment of South-eastern
Madagascar. We first examined whether seasons play a
role in affecting activity adjustments, social and postural
thermoregulation, and microhabitat selection separately.
For this, we compared between groups and among seasons the percentage of time spent resting (activity
adjustments), huddling (social thermoregulation), resting
in curled and prone positions (postural thermoregulation), and time spent in the upper canopy (microhabitat
selection). If seasonality is influential, we predicted that
lemurs would rest more and use huddling and curled
postures more frequently during cold seasons and would
spend more time in prone postures during warm periods.
We also expected lemurs to spend more time in the lower
layers of the forest during warm periods to get cooler
and use the upper levels more to warm up during cold
seasons. We further examined the role of seasonality by
modeling the simultaneous role of some climatic and dietary-related factors in determining frequencies of the
various types of behavioral thermoregulation in a multivariate analysis. Given the overall resource seasonality
of Madagascar, we predicted that lemur thermoregulaAmerican Journal of Physical Anthropology
Fig. 1. Average monthly temperature and rainfall at Sainte
Luce during the study period. Seasonal segments are indicated.
Tra-dry: transitional dry season.
tory behaviors would be shaped not only by climatic, but
also by dietary-related factors: when food is scarce or
has lower energy content lemurs should use energy saving behaviors more often.
MATERIALS AND METHODS
Study site and study species
Observations were conducted between December 1999
and January 2001 at the Sainte Luce Conservation Area
by GD, NB, and VM in a 377 ha fragment of the littoral
forest (24845’s 478110 E), 30 km north of Fort Dauphin
(South-eastern Madagascar). This forest, occurring within
2–3 km from the coast at an altitude of 0–20 m a s l, is
characterized by a tropical wet climate, with temperatures ranging from 15 to 308C and total annual rainfall of
2,480 mm. These littoral forests have a relatively open or
noncontinuous canopy, which is 6–12 m in height with
emergents up to 20 m (Bollen and Donati, 2005).
Though the area is characterized by an overall aseasonal climate, during the study period four climatic segments were identified: hot-wet (December–February), hotdry (March–May), cool-wet (June–August), and transitional-dry (September–November; see Fig. 1; Donati et al.,
2007). A month was considered wet when total rainfall
was above 100 mm (Morellato et al., 2000), cool when average 24-h temperature was below 218C (see Fig. 1).
Collared lemurs are cathemeral medium-sized primates (head-body length: 39–40 cm, tail length: 50–55 cm,
weight 2.3–2.5 kg). They are mostly frugivorous and live
in multimale-multifemale groups ranging from 3 to 17
individuals (Donati et al., 2007).
Behavioral data
Two groups of collared lemurs (Group A size: 8–13
individuals; Group B size: 4–6 individuals) were followed
3 days each month from 6:00 am to 6:00 pm. Group A
was followed during 13 months; Group B during 10
months, totaling 948 observation hours.
Individual identification was realized using nylon collars and colored pendants, and one individual per group
was radio-collared. Animal activity was recorded by the
instantaneous focal method (Altmann, 1974) at 5-min
intervals. Focal animals were chosen from all adult individuals in both study groups, and were rotated every 3
h, so that at the end of 3 observation days (12 observation h day21) all adult group members had been evenly
sampled. Truncated observations (very rare) were discarded when covering less than 70% of the respective
focal session. Active behaviors (feeding, foraging, mov-
BEHAVIORAL THERMOREGULATION IN COLLARED LEMURS
ing, and social behaviors), nonactive behaviors (resting
alone or huddling with one or more others), food type
consumed (mature and unripe fruits; mature and young
leaves; nectar; flowers; animal matter; other), and level
above ground (measured at 2-m intervals) were registered during observations.
The daily proportion of huddling with another animal
weighted by the total number of instantaneous records
was used to quantify social thermoregulation.
Resting postures were categorized as follow: 1) hunch:
the animal curled like a ball with the tail wrapped
around; 2) curl: as position 1 but with the tail hanging
down; 3) sit: stationary posture when the animal is
upright; 4) ventral prone: the animal lays on abdomen
with limbs and tail hanging down; 5) dorsal prone: the
animal lays on back with limbs and tail hanging down.
Postural thermoregulation was quantified using two
variables: the daily proportion of instantaneous observations in postures 1 and 2, ‘‘curled’’ postures, and the
daily proportion in postures 4 and 5, ‘‘prone’’ postures.
We excluded posture 3 from the analysis because its significance for thermoregulatory function was affected by
the fact that this posture is used during activities such
as feeding, grooming, inspecting, etc. When taken alone
posture 3 was often transitorily maintained for very
short periods, so it cannot be considered a purely
‘‘resting posture.’’
Microhabitat selection was quantified as the daily proportion of records in the canopy, i.e., above 6 m. This is
the lower limit of the forest canopy and the animals
were on average more exposed to meteorological factors
when resting/moving above this height. In a previous
study, we recorded appreciable differences in terms of
daily temperature and relative humidity between the
understory of the littoral forest and the canopy, i.e.,
larger fluctuations characterize the upper levels (up to
18C for temperatures and up to 10% for relative humidity; Donati and Borgognini, 2006).
Climatic data
357
Donati, 2005). The overall availability was obtained by
weighting the presence of a specific phenophase for
each species by its mean DBH. Diameter at breast
height has been demonstrated to be a reliable proxy of
the quantity of fruits produced by a tree (Ganzhorn,
2003).
All feeding trees used by the animals for more than
5 s were marked and identified via the help of a local
expert. On these occasions, tree height was measured
with a clinometer or estimated to the nearest meter
by eye.
Nutritional analyses were performed at the Department of Animal Ecology and Conservation of Hamburg
University. A total of 112 food samples representing all
the species eaten by collared lemurs during the study period were analyzed (in some cases one among the transect 78 species gave more than one food item, e.g.,
leaves, fruits, flowers, and some food species not present
in the phenological transects were also analyzed). Fresh
and dry weight was determined for each sample before
the analyses. Lipid content was determined by petroleum/ether extraction. Protein content was estimated by
the Biorad procedure. Soluble carbohydrates were
assessed after extraction with 50% methanol as the
equivalent of galactose after acid hydrolization (Ortmann
et al., 2006). Neutral detergent fiber content (NDF) was
determined according to van Soest (1994), modified
according to the instructions for use in an ‘‘Ankom fiber
analyzer.’’
To evaluate diet quality, we calculated the metabolizable energy in the monthly diet. We calculated the
weighted proportion of dry matter per month for each
nutritional compound, with the proportion of feeding
records for each food item as the weighted coefficient
(Kurland and Gaulin, 1987). Energy content from food
was obtained by standard conversion factors such as 4
kcal g21 for carbohydrate, 4 kcal g21 for crude protein
and 9 kcal g21 for lipid. We used a fiber conversion factor of 3 kcal g21 rather than 4 kcal g21 usually used for
carbohydrates, since the anaerobic microbes take 1
kcal g21 of fibers for their own growth during fermentation processes (Conklin-Brittain et al., 2006). The metabolizable energy was then obtained via the following
equation:
Temperature and relative humidity were registered at
2-h intervals by data loggers, Hobo H8 pro, operated by
custom software (BoxCar 3.51 for Windows, Onset Computer Corporation). Two data loggers were positioned at
1 and 10 m above ground level at the boundary between
the home ranges of the two study groups. Rainfall was
measured every day at 06.00 h using a rain gauge placed
near the camp. Daily data on wind velocity were registered by a station located at the Fort Dauphin airport
and kindly provided by the Direction Générale de la
Météorologie of Antananarivo. Solar radiation was not
considered in this study because of its believed limited
importance for forest-dwelling species (Hill et al., 2004).
where ME is the metabolizable energy per gram (in
kcal g21) of diet; L is the proportion of lipids; SP the proportion of soluble proteins; SC the proportion of soluble
carbohydrates and [NDF 3 0.415] the fraction of NDF
which are digested by brown lemurs (Campbell et al.,
2004).
Dietary-related data
Data analyses
To estimate variation in food availability, phenological
data were recorded for the plant species (n 5 78) whose
fruits were consumed by collared lemurs during the
study period. Diameter at breast height (DBH) was
measured for all the species used by the lemurs as feeding trees in two botanical transects covering 2,320 m 3
10 m. The first five adult (DBH 10 cm) individuals
for each tree species were selected in each transect to
collect phenological data. Trees were checked for the
presence/absence of fruits twice a month (Bollen and
The records of thermoregulatory activity were
weighted by the total number of instantaneous records.
Daily proportions were calculated for each group and
these data were log transformed to allow the use of multivariate parametric tests. As a first step, we evaluated
the influence of seasons in determining daily proportions
of each thermoregulatory behavior via a two-way
repeated measure ANOVA. Within-subjects factors were
the two groups and the four seasonal segments (hot-wet,
hot-dry, cool-wet, and transitional-dry).
ME ¼ ð9 3 LÞ ð4 3 SPÞ þ ð4 3 SCÞ þ ð3 3 ½NDF 3 0:415Þ
American Journal of Physical Anthropology
358
G. DONATI ET AL.
Second, we estimated the association between climatic
and dietary-related factors and the proportions of total
resting, huddling, postural thermoregulation, and microhabitat selection via Canonical Correlation Analysis
(CANCOR). CANCOR is suited for the mathematical
description of situations in which there are two sets of
variables obtained under the same conditions and the
objective is to study the relationship between these two
sets. This technique forms pairs of weighted linear combination of variables (latent roots), one in each set, such
that the correlation between the pair of latent roots is
maximized (McGarigal et al., 2000). The first set of variables, i.e., the predictor ones, included a group of climatic factors: daily average ambient temperature and
daily average relative humidity (both averaged over six
data points, as we used only observations from the 12
daylight hours), max daily wind speed, daily rainfall,
day length; and a group of dietary-related factors:
monthly metabolizable energy in the diet, daily proportion of feeding time, monthly fruit availability, monthly
average height of feeding trees (calculated averaging the
heights of all the trees used to feed during a given
month). The second set of variables, i.e., the dependent
ones, included: daily resting time (activity adjustments),
daily proportion of time in huddling (social thermoregulation), daily proportion of time in prone postures and
daily proportion of time in curled postures (postural
thermoregulation), daily proportion of time spent in the
upper canopy (microhabitat selection). Indices of perceived temperature were not included in the present
analysis because of their high correlation (Pearson: r [
0.8) with the original climatic variables and the consequent violation of the CANCOR model. We included feeding time in the independent data set and resting time in
the dependent data set because of the higher biological
priority of the former on the latter (sensu Hill et al.,
2003). All the variables used in the multivariate model
were numerical and entered the analysis after log or arcsin transformation to improve their linearity. The CANCOR model accepts variables measured with different
scales, i.e., both interval and ordinal variables.
RESULTS
Effect of seasons
Activity adjustments. During the study period Groups
A and B spent 53.4% 6 11.3% and 58.7% 6 9.9% of their
time resting, respectively (overall 56.1% 6 11.2% of the
total instantaneous records, N 5 11,376; Fig. 2a). Over
the four seasons, Group B reached a maximum of 66.3%
6 5.1% of its time inactive during the cool-wet season,
while the minimum was recorded in Group A during the
hot-wet season (41.5% 6 8.5%). A significant group effect
(F1,60 5 34.92, P 5 0.027) and an effect of seasons (F3,60
5 6.89, P 5 0.023) were observed.
Social thermoregulation. Overall, the two groups of
collared lemurs spent 31.3% 6 17.6% of their time in
huddling, with Group A devoting 29.4% 6 17.7% and
Group B 33.7% 6 17.3% of their time to this behavior
(Fig. 2b). Over the four seasons, the maximum time
spent in huddling was observed in Group A during the
transitional-dry season (44.6% 6 13.7%), while the minimum was recorded in the same group during the hot-wet
season (18.3% 6 13.9%). Only a major effect of seasons
was revealed (F3,65 5 4.49, P 5 0.025).
American Journal of Physical Anthropology
Postural thermoregulation. During the study period
the two groups spent 37.6% 6 16.7% and 6.4% 6 9.9% of
their time in curled and prone postures, respectively
(Fig. 2c,d). Curled postures peaked during the transitional-dry season in Group A (49.5% 6 14.4%) and
reached their minimum during the hot-dry season in
Group B (20.6% 6 16.9%). Conversely, prone postures
were observed more frequently during the hot-dry season in Group B (14.9% 6 14.5%), while they were almost
absent during the cool-wet season in Group A (0.2% 6
0.4%). A strong tendency to a seasonal effect (F3,65 5
3.41, P 5 0.053) and an interaction effect between
groups and seasons (F3,65 5 4.25, P 5 0.029) were found
for time spent in curled postures. Seasonal and group
effects were nonsignificant for time spent resting in
prone postures.
Microhabitat selection. The two groups spent 38.5% 6
27.1% of their time in the upper canopy (Fig. 2e). Group
A spent a greater proportion of time in the highest forest
layers, 45.8% 6 24.3%, than Group B, 28.9% 6 28.0%.
The animals were observed more frequently in the upper
canopy during the hot-dry season (Group B: 63.0% 6
19.8%), while this was infrequent during the hot-wet
season (Group B: 16.8% 6 26.3%). Time spent in the
higher part of the canopy and in the emergents did not
change significantly between the two groups and over
the four seasons.
Effect of climatic and dietary-related factors
Descriptive statistics showing the seasonal variation of
the nine variables represented by climatic and dietaryrelated seasonal factors (independent variables) and the
five variables represented by the four forms of behavioral thermoregulation (dependent variables) are illustrated in Table 1.
The first two pairs of latent roots derived from the canonical correlation between the set of independent variables and the set of dependent variables were highly significant (First root: v2 5 170.20, df 5 45, P \ 0.001, R2
5 89.30%; Second root: v2 5 66.28, df 5 32, P \ 0.001,
R2 5 56.10%). The redundancy analysis showed that the
first two pairs of latent roots together were able to
explain 56.61 and 34.21% of variance in the dependent
and independent sets of variables, respectively. Successive removal of latent roots did not give further significant inter-correlations. To understand the relationship
between the original variables and the composite variables created by the CANCOR model, the matrix of correlations between the first two pairs of roots and the original variables is shown in Table 2. The strength of the
association between each original variable and the roots
is given by the value of the correlation. Summarizing,
the first root shows that as feeding time, ambient temperature, day length, fruit availability, and height of
feeding trees decrease, resting time and proportion of
resting in huddling and in curled postures increase,
while time spent in prone posture decreases. The second
root shows that as quality of the diet and height of feeding trees decrease, the proportion of resting in huddling
and in curled postures increases, while time spent in the
upper canopy decreases. To visualize in two dimensions
the relationships among the above variables, we plotted
the score of each observation day in the new space created by the two latent roots in each set of variables (see
Fig. 3).
BEHAVIORAL THERMOREGULATION IN COLLARED LEMURS
359
Fig. 2. Mean percentage of time spent resting (a) and mean percentage of time spent in huddling (b), in curled postures (c), in
prone postures (d), and in the upper canopy (e) by the two study groups over the four seasonal segments. Tra-dry: transitional-dry
season. Error bars represent standard deviations.
DISCUSSION
The role of seasons
The tight relationship between time allocated to resting, resting postures and seasonal changes seems to be a
paramount thermoregulatory strategy and has been
repeatedly observed in studies on lemurs (Morland,
1993; Pereira et al., 1999), on other primates (Stelzner
and Hausfater, 1986; Schino and Troisi, 1990; Dasilva,
1993; Thompson et al., 1994; Bicca-Marquez and Calegaro-Marquez, 1998; Pochron, 2000; Hill et al., 2004;
Hill, 2006; Hanya et al., 2007; Campos and Fedigan,
2009; Kosheleff and Anderson, 2009), and on mammals
in general (Bradley and Hudson, 1974; Hasler and Sorenson, 1974; Körtner and Geiser, 2000). Our results
show that seasonal fluctuations had a major role in
shaping the four types of behavioral thermoregulation
used by collared lemurs. As predicted, resting time and
its proportion spent in postures which reduce the surface/volume ratio, i.e., huddling and curling, increased
during the colder seasons indicating that these strategies were used to minimize the dissipation of body heat.
By contrast, the proportion of time spent in prone,
extended postures was very low during the colder part of
the year and increased during the warm season, though
these differences were not statistically significant. This
is also a predicted result, since, following the same principle of surface/volume ratio body; elongation maximizes
dissipation of heat when the thermal environment is
particularly warm. Thus, together with activity adjustments and postural thermoregulation, social thermoregulation appears to have a relevant role in dealing with
American Journal of Physical Anthropology
360
G. DONATI ET AL.
TABLE 1. Means, standard deviations, and sample size of the 14 climatic, dietary-related, and behavioral variables used in the
canonical correlation model
Independent variables
Seasons
AT
Climatic factors
DL
RH
RF
Hot-wet
SD
n
Hot-dry
SD
n
Cool-wet
SD
n
Tra-dry
SD
n
25.3
1.0
20
24.9
1.3
14
19.7
1.1
18
22.7
1.7
13
13.5
0.2
20
11.4
0.5
14
10.9
0.3
18
12.6
0.7
13
93.3
3.9
17
89.9
7.0
10
96.1
2.7
15
89.5
6.1
13
3.1
4.8
17
2.6
6.4
10
13.6
31.1
15
0.6
0.7
13
WS
FT
12.1
3.2
17
14.2
4.6
10
15.0
4.8
15
18.0
5.5
13
27.4
5.2
20
21.4
6.3
14
19.2
2.4
18
18.7
1.3
13
Dependent variables
Dietary-related factors
ME
FA
HF
1.6
0.2
6
1.9
0.2
4
1.8
0.3
6
1.5
0.2
5
355.1
91.0
5
201.7
72.6
3
151.8
45.5
3
270.9
23.6
3
9.3
0.9
5
9.9
0.4
3
8.3
1.0
6
9.9
0.5
5
RT
Behavioral thermoregulation
HU
CP
PP
UC
51.2
6.4
20
59.8
8.0
20
69.1
7.0
18
66.3
7.9
13
23.8
17.9
20
21.4
14.5
20
40.2
12.0
18
41.1
16.4
13
27.9
14.5
20
32.1
17.8
20
45.5
9.8
18
47.7
16.5
13
10.2
11.8
20
9.6
11.4
20
3.5
7.5
18
1.2
3.2
13
34.4
28.8
20
56.4
19.3
20
35.1
29.5
18
30.5
21.8
13
AT: ambient temperature (8C); DL: day length; RH: relative humidity (%); RF: rainfall (mm); WS: wind speed (meters per second);
FT: feeding time (% of total records); ME: metabolizable energy in the diet (kcal); FA: fruit availability; HF: height of feeding trees
(meters); RT: resting time (% of total records); HU: resting in huddling; CP: resting in curled postures; PP: resting in prone postures; UC: time in the upper canopy; Tra-dry: transitional dry season.
TABLE 2. Pearson correlations between the first and the second latent roots derived from the canonical correlation and the original
variables in the two datasets
Independent set
1st Root
2nd Root
Dependent set
1st Root
2nd Root
Ambient temperature
Day length
Energy in the diet
Feeding time
Fruit availability
Height of feeding trees
Relative humidity
Rainfall
Wind speed
0.703
0.669
20.006
0.886
0.474
0.401
0.069
20.035
20.129
0.132
0.298
20.607
0.088
0.193
20.465
20.328
0.113
0.251
Resting in huddling
Resting in curled postures
Time in upper canopy
Resting in prone postures
Resting time
20.575
20.720
0.166
0.395
20.993
0.391
0.431
20.682
20.086
0.029
Significant correlations after Bonferroni adjustment are indicated in bold.
seasonal fluctuations. Only a few studies have shown the
association between huddling frequencies and seasons in
gregarious lemur species (Jolly, 1966; Tattersall, 1982; Pereira et al., 1999; Ostner, 2002). However, social thermoregulation seems to play an important role even for solitary ranging, nocturnal lemurs, which form day-time sleeping groups (Fietz and Dausmann, 2006). A large amount of
work has provided evidence that social thermoregulation
can be a source of substantial energy savings, since lower
metabolic rates due to huddling have been demonstrated
in many species of small mammals (Kauffman et al., 2003;
Kotze et al., 2008). It has been hypothesized, for example,
that one of the reasons why African four-striped grass
mice may sometimes occur in groups is that energetic benefits can be gained through huddling in habitats in which
food and water are scarce (Scantlebury et al., 2006). The
importance of social thermoregulation in lemurs has also
suggested the hypothesis that the unusual sex ratio found
in brown lemur groups, equal or male-biased (Kappeler,
2000), might be advantageous for possible thermoregulatory benefits given by extra males (Overdorff, 1998; Ostner,
2002). Our data collection was not designed to test this hypothesis, but in the larger study group, Group A, males
outnumbered females by 2:1. If animals huddle in proportion to their numbers, we would expect a greater huddling
frequency in Group A. However, we did not notice a tendency of the more numerous group, where several subordinate males were present, to participate more often in huddling than the smaller group.
American Journal of Physical Anthropology
Prone or upright body postures in sunny spots with
arms extended laterally are also used by primates to
gain heat (Jolly, 1966; Takemoto, 2004). Sunning or
basking in early morning is a common behavior in ringtailed lemurs, sifakas, and ruffed lemurs (Jolly, 1966;
Tattersall, 1982; Morland, 1993; Pereira et al., 1999).
Among anthropoids, wild Japanese macaques spend a
significant amount of time resting on the trees during
the winter to warm up (Hanya et al., 2007). However,
our data indicate that collared lemurs did not use basking or sunning as a thermoregulatory strategy in the littoral forest, and lying, prone postures were almost
absent during the winter. In a primary forest the only
opportunity for sunbathing is on the emergent part of
the canopy, where predation risk by diurnal raptors is
expected to be high. The absence of sunning behaviors in
collared lemurs is in line with other field studies on
Eulemur species (Sussman, 1974; Curtis et al., 1999; Pereira et al., 1999). Apparently, these taxa rely on other
strategies to warm up early in the morning. One of these
tactics could be the frequent use of social thermoregulation and curled postures, as this study seems to suggest.
Interestingly, the more egalitarian society and the high
degree of tolerance among brown lemurs as compared to
other lemurs (Kappeler, 1993; Pereira et al., 1999) could
favor social thermoregulation. Cathemerality has also
been suggested as a possible strategy to warm up by
being active during the coldest hours of the day, i.e.
before sunrise, in Eulemur species (Curtis et al., 1999).
BEHAVIORAL THERMOREGULATION IN COLLARED LEMURS
361
Fig. 3. Biplots of the scores of the observation days on the axes of the first latent root (a) and on the axes of the second latent
root (b) derived from the canonical correlation analysis. Abbreviations represent the original variables most associated with the
new canonical axes. The font size is in proportion to the strength of the correlation between the original variables and the canonical
roots. The arrows indicate the direction of increase of each original variable. AT: ambient temperature; DL: day length; FT: feeding
time; ME: metabolizable energy in the diet; FA: fruit availability; HF: height of feeding trees; RT: resting time; HU: resting in huddling; CP: resting in curled postures; PP: resting in prone postures; UC: time in the upper canopy. Open squares: hot-dry season;
open diamonds: hot-wet season; open triangles: cool-wet season; open circles: transitional-dry season.
Physiological data are necessary to test the latter hypothesis, but it seems that cathemeral activity in these
lemur species is triggered by multiple factors (Curtis
and Rasmussen, 2006; Donati et al., 2009).
As to differences between groups, our results also
show that Group A had significantly lower levels of resting than Group B. Group A occupied an interior, central
area of the fragment where the forest was relatively
undisturbed. Conversely, the home range of Group B
was located in the southern portion of the fragment
which was characterized by frequent use by local villagers due to the proximity to the nearby settlement and
the national road. The structural profile of these two
areas has been measured by the line-intersect technique
and significant differences in canopy cover were recorded
(Rakotondranary, 2004; Ganzhorn et al., 2007). If these
structural differences have resulted in micro-climatic differences, the higher level of resting of Group B might be
a general strategy to save energy in a more variable
thermal environment. Forest degradation and edge
effects have been repeatedly shown to modify densities,
ecology, and behavior of primates (Lovejoy et al., 1986;
Ganzhorn, 1995; Estrada and Coates-Estrada, 1996;
Onderdonk and Chapman, 2000; Lehman et al., 2006;
Rode et al., 2006). In degraded and logged areas animal
time-budget is altered and an increase of resting is often
observed (Johns, 1986; Cowlishaw and Dunbar, 2000).
However, climatic data from both areas and behavioral
records on a larger number of animals are a prerequisite
to verify the effects of such micro-climatic changes in the
Sainte Luce littoral forest.
The role of climatic and dietary-related factors
A relevant problem in examining further the role of
seasonal fluctuations in shaping behavioral thermoregulation is the difficulty in accounting for the variety of
factors which influence perceived temperatures and for
the effect of nonclimatic factors. As for climatic factors,
ambient temperature, humidity, solar radiation, and
wind speed have all been shown to influence behavior in
baboons (Stelzner and Hausfater, 1986; Pochron, 2000;
Hill and Dunbar, 2002; Hill et al., 2004; Hill, 2006), in
howler monkeys (Bicca-Marquez and Calegaro-Marquez,
1998), in capuchins (Campos and Fedigan, 2009), and in
chimpanzees (Kosheleff and Anderson, 2009). An index
of perceived environmental temperature that accounts
for the variation of climatic factors has also been proved
to be effective in predicting baboon’s resting and feeding
behavior (Hill et al., 2004). However, we did not use an
index of perceived temperature in our analysis because
of the unknown bias in applying an index developed for
humans to a species with very different thermal characteristics, such as the collared lemur. Among the climatic
variables, the CANCOR model indicates that ambient
temperature was the only climatic factor strongly associated with the set of thermoregulatory behaviors (Table
2). Thus, the animals spent more time resting, huddling,
and curling and less time in prone postures as temperature decreases. This result confirms that ambient temperature is a good predictor of the frequencies of thermoregulatory behaviors. Conversely, humidity and wind
speed did not emerge as important climatic factors, perhaps because of their relatively low fluctuations in the
littoral forest environment (Donati and Borgognini,
2006). Based on captive studies, the thermoneutral zone
of E. fulvus, a species closely related to E. collaris, is
placed between 22 and 308C (Daniels, 1984). Mean minimum temperatures recorded at Sainte Luce were below
the thermoneutral zone for both the cool-wet and the
transitional-dry seasons (see Fig. 1). This means that
thermoregulatory tactics would be needed primarily to
counteract cold stress and to maintain a high body temperature during the coolest segments of the year.
Not surprisingly, given the relatively southern latitude
of Sainte Luce, the CANCOR model indicates that day
American Journal of Physical Anthropology
362
G. DONATI ET AL.
length also had a relevant role in shaping thermoregulatory responses. This result apparently matches observations on South-African baboons, where variations in day
length are one of the primary factors influencing thermoregulatory responses, since long days relax the foraging
constraints over the midday periods (Hill et al., 2003;
Hill, 2006). But we found an opposite trend in collared
lemurs, since resting time and postural thermoregulation increase as day length decreases. This result could
be explained by the strong association of day length with
both temperature and phenological cycles at Sainte Luce
(Bollen and Donati, 2005), making it difficult to separate
the effect of the former from those of the latter factors,
even when using multivariate statistics. Furthermore,
day length effects are difficult to evaluate in a cathemeral lemur, which is not constrained by a single phase of
the 24-h cycle (Curtis and Donati, in press).
The CANCOR model shows that two dietary-related
variables, i.e., feeding time and the availability of metabolizable energy in the diet, had very strong associations
with the set of thermoregulatory behaviors. In particular, the proportion of resting and the frequency of huddling and curled postures increased as feeding time and
energy from the diet decreased (Table 2). The other two
dietary-related variables used in our model, fruit availability and height of feeding trees, were also correlated
to the thermoregulatory behaviors, though by a weaker
association if compared to energy from diet and feeding
time. Fruit availability seems to behave in a similar way
as feeding time; while the height of feeding trees, not
surprisingly, is most associated with the time spent in
the upper canopy by a positive relationship. Thus, as
predicted, non climatic, dietary-related factors had a relevant role in shaping not only activity adjustments, but
also social and postural thermoregulation. While diet
has been often identified as a significant factor in shaping anthropoid (Dasilva, 1992; Milton, 1998; Hill and
Dunbar, 2002) and lemur activity-budget (Engqvist and
Richard, 1991; Ganzhorn, 2002; Ganzhorn et al., 2003;
Tarnaud, 2006; Donati et al., 2009), it has rarely been
analyzed in relation to specific thermoregulatory behaviors in the field. Dasilva (1993) has shown that postural
changes of Colobus polykomos are not solely related to
climate, but they also reflect food availability and energy
content of food consumed. Pochron (2000) hypothesized
that baboons could not afford micro-habitat selection
during their activities in the dry season because of the
constraints of low food availability. In captivity, changes
of food provisioning act as a triggering mechanism for
hypothermia and the occurrence of daily torpor in Microcebus spp. (Aujard et al., 1998; Genin and Perret, 2000).
An important role of the diet in determining the proportion of thermoregulatory behaviors in lemurs was
expected for a number of reasons. First, Malagasy
lemurs are known to face long seasonal bottle-necks in
terms of food availability both in the western seasonal
forests (Sorg and Rohner, 1996; Bollen et al., 2005) and
in the eastern rainforests (Wright, 1999; Bollen and Donati, 2005; Wright et al., 2005). These wide fluctuations
are likely to expose frugivorous lemurs to periodic timewindows of limited energy intake (Ganzhorn et al., 2003;
but see Curtis, 2004). Some of the most striking adaptations to seasonality found in lemurs, such as torpor,
have already been related to this phenomenon (Wright,
1999; Fietz and Dausmann, 2006). Second, all lemur species studied so far are hypometabolic (Genoud, 2002;
Simmen et al., 2010), which could also be interpreted as
American Journal of Physical Anthropology
an adaptation to scarce and unpredictable resources
(Kurland and Pearson, 1986; McNab, 1986). However, in
captivity the low metabolic rate of Eulemur species
seems to be associated with high body temperatures
(Daniels, 1984; Müller, 1985), which would explain the
overall high levels of activity typical of brown lemurs
(Donati et al., 2007). If such a pattern holds true in the
wild as well, it means that these lemurs have evolved
physiological and possibly behavioral traits to keep high
body temperatures in spite of their low metabolic rate.
The output of our multivariate model shows that proportion of resting, huddling, and postural thermoregulation
are all behaviors associated with climatic and dietaryrelated fluctuations in collared lemurs. Therefore, these
results suggest that lemurs rely on activity and postural
adjustments, but also on social thermoregulation to compensate for seasonal environmental variations.
ACKNOWLEDGMENTS
This study was carried out under the collaboration
agreement between the Departments of Animal Biology
and Anthropology of the University of Antananarivo,
the Institute of Zoology of Hamburg University and
QIT Madagascar Minerals. The authors thank the Commission Tripartite of the Malagasy Government, the
Ministère des Eaux et Forêts, and QMM for their collaboration and permissions to work in Madagascar.
They thank Joerg Ganzhorn for his continuous scientific
support. They acknowledge Manon Vincelette, JeanBaptiste Ramanamanjato, and Laurent Randriashipara
for providing help at various stages of this research.
They are grateful to An Bollen for providing additional
data on collared lemur ecology. Many thanks to Dauphin Mbola, Givé Sambo, Ramisy Edmond, the local
assistants who helped with the collection of behavioral
and phenology data. Irene Tomaschewsky helped with
plant analyses.
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factors, effect, behavior, dietary, climatico, lemur, collaris, thermoregulatory, eulemur, related, gregarious
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